Dynamics and regulation of contractile actin-myosin networks in morphogenesis.

Abstract

Contractile actin-myosin networks generate forces that drive cell shape changes and tissue remodeling during development. These forces can also actively regulate cell signaling and behavior. Novel features of actin-myosin network dynamics, such as pulsed contractile behaviors and the regulation of myosin localization by tension, have been uncovered in recent studies of Drosophila. In vitro studies of single molecules and reconstituted protein networks reveal intrinsic properties of motor proteins and actin-myosin networks, while in vivo studies have provided insight into the regulation of their dynamics and organization. Analysis of the complex behaviors of actin-myosin networks will be crucial for understanding force generation in actively remodeling cells and the coordination of cell shape and movement at the tissue level.

(a) A single non-muscle myosin II motor translocates toward the plus end of an actin filament (left). However, it has a low duty ratio and thus spends only a small fraction of its time bound to the actin filament. Because of this, the motor is non-processive and does not move continuously along the actin filament for long distances. Gray arrow indicates the direction of motor movement. (b) Several myosin motors can assemble into a processive, bipolar filament that generates relative movement between two anti-parallel actin filaments. Gray arrows indicate the direction of actin filament movement. (c) A contractile network formed from many actin filaments and bipolar myosin filaments. Myosin motor activity causes the network to contract.

(a) Prospective mesoderm cells on the ventral surface of the Drosophila embryo constrict their apical surfaces. This generates a bend in the tissue that causes the cells to invaginate to form a ventral furrow (dark gray). These cell shape changes are associated with an apical actin-myosin network (red). Before (top) and during (bottom) furrow formation. Lateral views, anterior left, ventral down (left), cross-sections (right). (b) Apical actin-myosin networks (red) also drive apical constriction of amnioserosa cells (dark gray), which generates one force that pulls the lateral epidermis closed over the dorsal surface of the Drosophila embryo. Contraction of the leading edge cable (thick red line), amnioserosa cell death, and filopodial protrusions also contribute to dorsal closure. (c) A medial actin-myosin network that spans the apical cell surface (light red) is connected through a second, junctional population that is anchored to adherens junctions at cell-cell contacts (dark red). (d) Recent studies demonstrate that apical constriction occurs in brief pulses associated with fluctuations in the actin-myosin network. Apical constriction is closely correlated with bursts of myosin accumulation.